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History. All rights reserved.”
1
ABSTRACT ..............................................................................................................3
LEARNING OBJECTIVES .....................................................................................3
PART A: INTRODUCTION AND THEORY ........................................................................4
1. INTRODUCTION ................................................................................................4
WHAT IS A SPECIES’ DISTRIBUTION MODEL? ........................................................4
2. THEORETICAL FRAMEWORK...............................................................................8
GEOGRAPHICAL VERSUS ENVIRONMENTAL SPACE................................................8
ESTIMATING NICHES AND DISTRIBUTIONS ..........................................................11
USES OF SPECIES’ DISTRIBUTION MODELS ........................................................15
PART B: DEVELOPING A SPECIES’ DISTRIBUTION MODEL .............................................17
3. DATA TYPES AND SOURCES .............................................................................17
BIOLOGICAL DATA ...........................................................................................19
ENVIRONMENTAL DATA ...................................................................................21
4. MODELING ALGORITHMS .................................................................................22
DIFFERENCES BETWEEN METHODS AND SELECTION OF ‘BEST’ MODELS ................27
5. ASSESSING PREDICTIVE PERFORMANCE ...........................................................28
STRATEGIES FOR OBTAINING TEST DATA ...........................................................28
THE PRESENCE/ABSENCE CONFUSION MATRIX ..................................................30
SELECTING THRESHOLDS OF OCCURRENCE ......................................................34
THRESHOLD-INDEPENDENT ASSESSMENT .........................................................37
CHOOSING A SUITABLE TEST STATISTIC ............................................................39
PART C: CASE STUDIES ..........................................................................................40
CASE STUDY 1: PREDICTING DISTRIBUTIONS OF KNOWN AND UNKNOWN SPECIES IN
MADAGASCAR (BASED ON RAXWORTHY ET AL., 2003)............................................40
ACKNOWLEDGEMENTS ...........................................................................................44
REFERENCES ........................................................................................................44
2
Species’ Distribution Modeling for Conservation
Educators and Practitioners
Richard G. Pearson
Center for Biodiversity and Conservation & Department of Herpetology
American Museum of Natural History
ABSTRACT
Models that predict distributions of species by combining known occurrence
records with digital layers of environmental variables have much potential for
application in conservation. Through using this module, teachers will enable
students to develop species’ distribution models, to apply the models across a
series of analyses, and to interpret predictions accurately. Part A of the synthesis
introduces the modeling approach, outlines key concepts and terminology, and
describes questions that may be addressed using the approach. A theoretical
framework that is fundamental to ensuring that students understand the uses and
limitations of the models is then described. Part B of the synthesis details the
main steps in building and testing a distribution model. Types of data that can be
used are described and some potential sources of species’ occurrence records
and environmental layers are listed. The variety of alternative algorithms for
developing distribution models is discussed, and software programs available to
implement the models are listed. Techniques for assessing the predictive ability
of a distribution model are then discussed, and commonly used statistical tests
are described. Part C of the synthesis describes three case studies that illustrate
applications of the models: i) Predicting distributions of known and unknown
species in Madagascar; ii) Predicting global invasions by plants of South African
origin; and iii) Modeling the potential impacts of climate change on species’
distributions in Britain and Ireland.
This module is targeted at a level suitable for teaching graduate students and
conservation professionals.
Learning objectives
Through use of this synthesis, teachers will enable students to
3
2. Run a distribution model using appropriate data and methods
3. Test the predictive performance of a distribution model
4. Apply distribution models to address a range of conservation questions
This synthesis aims to provide an overview of the theory and practice of species’
distribution modeling. Through use of the synthesis, teachers will enable students
to understand the theoretical basis of distribution models, to run models using a
variety of approaches, to test the predictive ability of models, and to apply the
models to address a range of questions. Part A of the synthesis introduces the
modeling approach and describes the usefulness of the models in addressing
conservation questions. Part B details the main steps in building a distribution
model, including selecting and obtaining suitable data, choosing a modeling
algorithm, and statistically assessing predictive performance. Part C of the
synthesis provides three case studies that demonstrate uses of species’
distribution models.
4
The environmental conditions that are suitable for a species may be
characterized using either a mechanistic or a correlative approach. Mechanistic
models aim to incorporate physiologically limiting mechanisms in a species’
tolerance to environmental conditions. For example, Chuine and Beaubien
(2001) modeled distributions of North American tree species by estimating
responses to environmental variables (including mean daily temperature, daily
precipitation, and night length) using mechanistic models of factors including frost
injury, phenology, and reproductive success. Such mechanistic models require
detailed understanding of the physiological response of species to environmental
factors and are therefore difficult to develop for all but the most well understood
species.
Correlative models aim to estimate the environmental conditions that are suitable
for a species by associating known species’ occurrence records with suites of
environmental variables that can reasonably be expected to affect the species’
physiology and probability of persistence. The central premise of this approach is
that the observed distribution of a species provides useful information as to the
environmental requirements of that species. For example, we may assume that
our plant species of interest favors wet clay soils because it has been observed
growing in these soils. The limitations of this approach are discussed later in the
synthesis, but it has been demonstrated that this method can yield valuable
biogeographical information (e.g., Bourg et al., 2005; Raxworthy et al., 2003).
Since spatially explicit occurrence records are available for a large number of
species, the vast majority of species’ distribution models are correlative. The
correlative approach to distribution modeling is the focus of this synthesis.
5
Figure 1. Flow diagram detailing the main steps required for building and validating a correlative species distribution model.
6
The species occurrence records and environmental variables are entered into an
algorithm that aims to identify environmental conditions that are associated with
species occurrence. If just one or two environmental variables were used, then
this task would be relatively straightforward. For example, we may readily
discover that our plant species has only been recorded at localities where mean
monthly precipitation is above 60mm and soil clay content is above 40%. In
practice, we usually seek algorithms that are able to integrate more than two
environmental variables, since species are in reality likely to respond to multiple
factors. Algorithms that can incorporate interactions among variables are also
preferable (Elith et al. 2006). For example, a more accurate description of our
plant’s requirements may be that it can occur at localities with mean monthly
precipitation between 60mm and 70mm if soil clay content is above 60%, and in
wetter areas (>70mm) if clay content is as low as 40%.
A number of modeling algorithms that have been applied to this task are
reviewed in Section 4. Depending on the method used, various decisions and
tests will need to be made at this stage to ensure the algorithm gives optimal
results. For example, a suitable ‘regularization’ parameter will need to be
selected if applying the Maxent method (see Phillips et al. 2006, and Box 3), or
the degrees of freedom must be selected if running a generalized additive model
(see Guisan et al. 2002). The relative importance of alternative environmental
predictor variables may also be assessed at this stage so as to select which
variables are used in the final model.
Having run the modeling algorithm, a map can be drawn showing the predicted
species’ distribution. The ability of the model to predict the known species’
distribution should be tested at this stage. A set of species occurrence records
that have not previously been used in the modeling should be used as
independent test data. The ability of the model to predict the independent data is
assessed using a suitable test statistic. Different approaches to generating test
datasets and alternative statistical tests are discussed in Section 5. Since a
number of modeling algorithms predict a continuous distribution of environmental
suitability (i.e. a prediction between 0 and 1, as opposed to a binary prediction of
‘suitable’ or ‘unsuitable’), it is sometimes useful to convert model output into a
prediction of suitable (1) or unsuitable (0). This is a necessary step before
applying many test statistics; thus, methods for setting a threshold probability,
above which the species is predicted as present, are also outlined in Section 5.
Once these steps have been completed, and if model validation is successful,
the model can be used to predict species’ occurrence in areas where the
distribution is unknown. Thus, a set of environmental variables for the area of
interest is input into the model and the suitability of conditions at a given locality
is predicted. In many cases the model is used to ‘fill the gaps’ around known
occurrences (e.g., Anderson et al., 2002a; Ferrier et al., 2002). In other cases,
the model may be used to predict species’ distributions in new regions (e.g. to
7
study invasion potential, for review see Peterson 2003) or for a different time
period (e.g. to estimate the potential impacts of future climate change, for review
see Pearson and Dawson, 2003). Three examples of the use of predictions from
species distribution models are presented in Part C. Ideally, model predictions
into different regions of for different time periods should be tested against
observed data; for example, Thuiller et al. (2005; see case study 2) tested
predictions of invasion potential using occurrence records from the invaded
distribution, whilst Araújo et al. (2005a) tested predictions of distribution shifts
under climate change using observed records from different decades.
2. THEORETICAL FRAMEWORK
This section outlines some of the fundamental concepts that are crucial for
understanding how species’ distribution models work, what types of questions
they are suitable for addressing, and how model output should be interpreted.
8
about the species’ actual distribution; the species is likely to occur in other areas
in which it has not yet been detected (e.g., Fig. 2, area A). If the actual
distribution is plotted in environmental space then we identify that part of
environmental space that is occupied by the species, which we can define as the
occupied niche.
9
The distinction between the occupied niche and the fundamental niche is similar,
but not identical, to Hutchinson’s (1957) distinction between the realized niche
and the fundamental niche. With reference to the case of two species utilizing a
common resource, Hutchinson described the realized niche as comprising that
portion of the fundamental niche from which a species is not excluded due to
biotic competition. The definition of the occupied niche used in this synthesis
broadens this concept to include geographical and historical constraints resulting
from a species’ limited ability to reach or re-occupy all suitable areas, along with
biotic interactions of all forms (competition, predation, symbiosis and parasitism).
Thus, the occupied niche reflects all constraints imposed on the actual
distribution, including spatial constraints due to limited dispersal ability, and
multiple interactions with other organisms.
10
dispersal ability, such as birds. In such cases it is useful to only utilize records for
modeling that are known to be from breeding distributions, rather than migrating
individuals. Because correlative species distribution models utilize observed
species occurrence records to identify suitable habitat, inclusion of occurrence
localities from sink populations is problematic. However, it is often assumed that
observations from source areas will be much more frequent than observations
from sink areas, so this source of potential error is commonly overlooked.
One more thing to be aware of before we move on is that some studies explicitly
aim to only investigate one part of the fundamental niche, by using a limited set
of predictor variables. For example, it is common when investigating the potential
impacts of future climate change to focus only on how climate variables impact
species’ distributions. A species’ niche defined only in terms of climate variables
may be termed the climatic niche (Pearson and Dawson, 2003), which
represents the climatic conditions that are suitable for species existence. An
approximation of the climatic niche may then be mapped in geographical space,
giving what is commonly termed the bioclimate envelope (Huntley et al., 1995;
Pearson and Dawson, 2003).
Let us first ask what the aim of the modeling is: what element of a species’
distribution are we trying to estimate? There are many potential uses of the
approach (Table 1) and these require modeling either the actual distribution or
the potential distribution. For example, if a model is being used with the purpose
of selecting sites that should be given high conservation priority, then modeling
the actual distribution will be the aim (since there would be less priority given to
conserving sites where the environment is suitable for the species, but the
species is not present). In contrast, if the purpose is to identify sites that may be
suitable for the reintroduction of an endangered species, then modeling the
potential distribution is an appropriate aim. We will now consider the degree to
which alternative aims are achievable using the species’ distribution modeling
approach.
11
Table 1. Some published uses of species’ distribution models in conservation biology
12
occurrence records are available, perhaps due to limited survey effort
(Anderson and Martinez-Meyer, 2004) or low probability of detection
(Pearson et al., 2007), the available records are unlikely to provide a
sufficient sample to enable the full range of environmental conditions
occupied by the species to be identified. In other cases, surveys may
provide extensive occurrence records that provide an accurate picture as
to the environments inhabited by a species in a particular region (for
example, breeding bird distributions in the United Kingdom and Ireland are
well known; Gibbons et al., 1993). It should be noted that there is not
necessarily a direct relationship between sampling in geographical space
and in environmental space. It is quite possible that poor sampling in
geographical space could still result in good sampling in environmental
space.
13
Figure 3. Diagram illustrating how a hypothetical species’ distribution model may be fitted to
observed species occurrence records (using the same hypothetical case as in Fig. 2). A
modelling technique (e.g. GARP, Maxent) is used to characterize the species’ niche in
environmental space by relating observed occurrence localities to a suite of environmental
variables. Notice that, in environmental space, the model may not identify either the species’
occupied niche or fundamental niche; rather, the model identifies only that part of the niche
defined by the observed records. When projected back into geographical space, the model will
identify parts of the actual distribution and potential distribution. For example, the model
14
projection labeled 1 identifies the known distributional area. Projected area 2 identifies part of the
actual distribution that is currently unknown; however, a portion of the actual distribution is not
predicted because the observed occurrence records do not identify the full extent of the occupied
niche (i.e. there is incomplete sampling; see area D in Fig. 2). Similarly, modeled area 3 identifies
an area of potential distribution that is not inhabited (the full extent of the potential distribution is
not identified because the observed occurrence records do not identify the full extent of the
fundamental niche due to, for example, incomplete sampling, biotic interactions, or constraints on
species dispersal; see areas D and E in Fig. 2).
Consider now predicted area 3 in Fig. 3. Here, the model identifies an area of
potential distribution that is environmentally similar to where the species is known
to occur, but which is not inhabited. The full extent of the potential distribution is
not predicted, but the model can be useful for identifying sites that may be
suitable for reintroduction of a species (Pearce and Lindenmayer, 1998) or sites
where a species is most likely to become invasive (if it overcomes dispersal
barriers and if biotic competition does not prevent establishment; Peterson,
2003). Model predictions of this type also have the potential to accelerate the
discovery of previously unknown species that are closely related to the modeled
species and that occupy similar environmental space but different geographical
space (Raxworthy et al., 2003; see Case Study 1).
15
areas that are isolated from observed occurrence records by a dispersal barrier
may be removed (Peterson et al., 2002) and the influence of competing species
may be incorporated (Anderson et al., 2002b).
The discussion in this section should help clarify the theoretical basis of the
species’ distribution modeling approach. It is crucial that any application of these
models has a sound theoretical basis and that model outputs are interpreted in
the context of this framework (see Box 1). It should now be apparent why the
terminology used to describe these models is so varied throughout the literature.
The terms ‘ecological niche model’, ‘environmental niche model’, ‘bioclimate
envelope model’ and ‘environmental suitability model’ usually refer to attempts to
estimate the potential distribution of a species. Use of the term ‘species
distribution model’ implies that the aim is to simulate the actual distribution of the
species. Nevertheless, each of these terms refers to the same basic approach,
which can be summarized as follows: 1) the study area is modeled as a raster
map composed of grid cells at a specified resolution, 2) the dependent variable is
the known species’ distribution, 3) a suite of environmental variables are collated
to characterize each cell, 4) a function of the environmental variables is
generated so as to classify the degree to which each cell is suitable for the
species (Hirzel et al., 2002). Part B of this synthesis details the principal steps
required to build a distribution model, including selecting and obtaining suitable
data, choosing a modeling algorithm, and statistically assessing predictive
performance.
16
Box 1. Caution! On the use and misuse of models
Garbage in, garbage out: This old adage is as relevant to distribution
modeling as it is to other fields. Put simply, a model is only as good as the
data it contains. Thus, if the occurrence records used to build a correlative
species’ distribution model do not provide useful information as to the
environmental requirements of the species, then the model cannot provide
useful output. If you put garbage into the model, you will get garbage out.
Model extrapolation: ‘Extrapolation’ refers to the use of a model to
make predictions for areas with environmental values that are beyond the
range of the data used to calibrate (i.e. develop) the model. For example,
suppose a distribution model was calibrated using occurrence records that
spanned a temperature range of 10–20oC. If the model is used to predict
the species’ distribution in a different region (or perhaps under a future
climate scenario) where the temperature reaches 25oC, then the model is
extrapolating. In this case, because the model has no prior information
regarding the probability of the species’ occurrence at 25oC, the prediction
may be extremely uncertain (see Pearson et al., 2006). Model
extrapolation should be treated with a great deal of caution.
The lure of complicated technology: Many approaches to modeling
species’ distributions utilize complex computational technology (e.g.
machine learning tools such as artificial neural networks and genetic
algorithms) along with huge GIS databases of digital environmental layers.
In some cases, these approaches can yield highly successful predictions.
However, there is a risk that model users will be swayed by the apparent
complexity of the technology: ‘it is so complicated, it must be correct’!
Always remember that a model can only be useful if the theoretical
underpinnings on which it is based are sound.
For additional discussion of the limitations of ecological models, see
the NCEP module Applications of remote sensing to ecological modeling.
17
(termed ‘raster’ data; e.g. land cover types derived from remote sensing [see
NCEP module Remote sensing for conservation biology]). For use in a
distribution model, it is usual to reformat all environmental data to a raster grid.
For example, temperature records from weather stations may be interpolated to
give continuous data over a grid (Hijmans et al. 2005). Formatting all data to the
same raster grid ensures that environmental data are available for every cell in
which biological data have been recorded. These cells, containing both biological
data and environmental data, are used to build the species’ distribution model.
After the model is constructed, its fit to test occurrence records is evaluated (see
section 5) and, if the fit is judged to be acceptable, the occurrence of species in
cells for which only environmental data are available can be predicted. Note that
in some applications the model may be used to predict the species’ distribution in
a region from which data were not used to build the model (e.g. to predict the
spread of an invasive species) or under a future climate scenario. In these cases,
environmental data for the new region or climate scenario must also be collated.
Table 2. Some example sources of biological and environmental data for use in species’
distribution modeling.
18
A consideration when collating data is the spatial scale at which the model will
operate. Spatial scale has two components: extent and resolution (see NCEP
module Applications of remote sensing to ecological modeling). Extent refers to
the size of the region over which the model is run (e.g. New York state or the
whole of North America) whilst resolution refers to the size of grid cells (e.g. 1km2
or 10km2). Note that it is common for datasets with large extent to have coarse
resolution (e.g. data for North America at 10km2) and datasets with small extent
to have fine resolution (e.g. New York state at 1km2). Spatial scale can play an
important role in the application of a species’ distribution model. In particular,
ideally the data resolution should be relevant to the species under consideration:
the appropriate data resolution for studying ants is likely to be very different from
that for studying elephants.
Biological data
Data describing the known distribution of a species may be obtained in a variety
of ways:
19
2) Large surveys: distribution information may be available from surveys
undertaken by a large number of people. For example, Araújo et al.
(2005a) built distribution models using data from The new atlas of
breeding birds in Britain and Ireland: 1988-1991 (Gibbons et al., 1993),
which represents the sampling effort of hundreds of volunteers.
3) Museum collections: occurrence localities can be obtained from
collections in natural history museums. For example, Raxworthy et al.
(2003) utilized occurrence records of chameleons in Madagascar that are
held in museum collections.
4) Online resources: distributional data from a variety of sources are
increasing being made available over the internet (see Table 2). For
example, the Global Biodiversity Information Facility (www.gbif.org) is
collating available datasets from a diversity of sources and making the
information available online via a searchable web portal.
There are a number of additional potential sources of bias and error that should
be carefully considered when collating species’ distribution data. Errors may
arise through the incorrect identification of species, or inaccurate spatial
referencing of samples. Biases can also be introduced because collectors tend to
sample in easily accessible locations, such as along roads and rivers and near
towns or biological stations (Graham et al., 2004a). In some cases, biased
sampling in geographical space may lead to non-representative sampling of the
available environmental conditions, although this is not necessarily the case.
When utilizing records from museum collections, it should be remembered that
these data were not generally collected with the purpose of determining the
distributional limits of a species; rather, sampling for museum collections tends to
be biased toward rare and previously unknown species.
20
Environmental data
A wide range of environmental input variables have been employed in species’
distribution modeling. Most common are variables relating to climate (e.g.
temperature, precipitation), topography (e.g., elevation, aspect), soil type and
land cover type (see Table 2). Variables tend to describe primarily the abiotic
environment, although there is potential to include biotic interactions within the
modeling. For example, Heikkinen et al. (2007) used the distribution of
woodpecker species to predict owl distributions in Finland since woodpeckers
excavate cavities in trees that provide nesting sites for owls.
Environmental variables may comprise either continuous data (data that can take
any value within a certain range, such as temperature or precipitation) or
categorical data (data that are split into discrete categories, such as land cover
type or soil type). Categorical data cannot be used with a number of common
modeling algorithms (see Section 4). In these cases, it may be possible to
generate a continuous variable from the categorical data. For example, Pearson
et al. (2002) estimated soil water holding capacity from categorical soil data, and
used these values within a water balance model to generate continuous
predictions of soil moisture surplus and deficit.
21
variables, although some of these variables are likely to have been rejected by
the algorithm applied because they did not provide useful information beyond
that which was included in other variables).
4. MODELING ALGORITHMS
A number of alternative modeling algorithms have been applied to classify the
probability of species’ presence (and absence) as a function of a set of
environmental variables. The task is to identify potentially complex non-linear
relationships in multi-dimensional environmental space. In Section 2 we assumed
that the modeling algorithm is excellent, enabling us to identify three expected
types of model prediction, illustrated by modeled areas 1, 2 and 3 in Fig. 3. If we
now admit some degree of error in the algorithm’s ability to fit the observed
records, then a fourth type of prediction will occur: the model will predict as
suitable areas that are part of neither the actual nor the potential distribution. The
most useful algorithms will limit these erroneous ‘type 4’ predictions.
Table 3 lists some commonly used approaches for species’ distribution modeling.
Some methods that have been applied are statistical (e.g. generalized linear
models [GLMs] and generalized additive models [GAMs]), whilst other
approaches are based on machine-learning techniques (e.g., maximum entropy
[Maxent] and artificial neural networks [ANNs]). Published studies have often
applied one or more of these algorithms and have given the resulting model a
name or acronym (e.g., ‘Maxent’ refers to an implementation of the maximum
entropy method, whilst ‘BIOMOD’ is the acronym given to a model that
implements a number of methods, including GLMs and GAMs). Often these
models have been implemented in user-friendly software that is free and easy to
obtain (Table 3).
22
Table 3. Some published methods for species’ distribution modeling.
1
‘Method’ refers to a statistical or machine-learning technique. 2 ‘Model/software name’ refers to a name (or acronym) given to a published model
that implements the method(s) stated. Software to implement the method for species’ distribution modeling is readily available at no cost for those
models marked with an asterisk (*); other models are available at the discretion of the author(s). 3 The genetic algorithm for rule-set prediction
(GARP) includes within its processing multiple methods, including GLM. 4 Note that Pseudo-absence here refers to the sampling approach
implemented in the GARP software; in principle, any presence-absence method can be implemented using pseudo absences. 5 R is a freely
available (at no cost) software environment for statistical computing and graphics (http://www.r-project.org/).
Based in part on Elith et al. (2006) and Guisan and Thuiller (2005).
23
There are some important differences between among model algorithms that
should be carefully considered when selecting which method(s) to apply. One
key factor is whether the algorithm requires data on observed species absence
(Section 3). Some algorithms operate by contrasting sites where the species has
been detected with sites where the species has been recorded as absent (e.g.,
GLMs, GAMs, ANNs). However, reliable absence data often are not available
(Section 3), so other methods have been applied that do not require absence
data. We can distinguish three types of presence-only methods:
24
contribution of each input variable to the prediction is difficult (sensitivity analysis
may be used, but this requires additional analyses). In contrast, a GLM builds a
regression equation from which the relative contributions of different variables
are immediately apparent (Guisan et al., 2002).
It is not possible within the scope of this synthesis to describe the theory,
advantages and disadvantages of a large number of modeling algorithms; the
reader is referred to the literature cited in Table 3. However, see Box 3 and the
practical exercise by Steven Phillips that accompanies this Synthesis for a more
detailed description of one method, Maxent.
25
Box 3. Maximum Entropy (Maxent) modeling of species distributions
(based on Phillips et al., 2006)
Maxent is a general-purpose method for characterizing probability
distributions from incomplete information. In estimating the probability
distribution defining a species’ distribution across a study area, Maxent
formalizes the principle that the estimated distribution must agree with
everything that is known (or inferred from the environmental conditions
where the species has been observed) but should avoid making any
assumptions that are not supported by the data. The approach is thus to
find the probability distribution of maximum entropy (the distribution that is
most spread-out, or closest to uniform) subject to constraints imposed by
the information available regarding the observed distribution of the species
and environmental conditions across the study area.
The Maxent method does not require absence data for the species
being modeled; instead it uses background environmental data for the
entire study area. The method can utilize both continuous and categorical
variables and the output is a continuous prediction (either a raw probability
or, more commonly, a cumulative probability ranging from 0 to 100 that
indicates relative suitability). Maxent has been shown to perform well in
comparison with alternative methods (Elith et al., 2006; Pearson et al.,
2007; Phillips et al., 2006). One drawback of the Maxent approach is that
it uses an exponential model that can predict high suitability for
environmental conditions that are outside the range present in the study
area (i.e. extrapolation, see Box 1). To alleviate this problem, when
predicting for variable values that are outside the range found in the study
area, these values are reset (or ‘clamped’) to match the upper or lower
values found in the study area.
For a concise mathematic definition of Maxent and for more detailed
discussion of its application to species distribution modeling see Phillips et
al. (2004, 2006). These authors have developed software with a user-
friendly interface to implement the Maxent method for modeling species
distributions (for free download see web link in Table 3). The software also
calculates a number of alternative thresholds (see Section 5), computes
model validation statistics (see Section 5), and enables the user to run a
jackknife procedure to determine which environmental variables contribute
most to the model prediction (see the practical exercise by Steven Phillips
that accompanies this synthesis).
The model algorithm is in some ways the ‘core’ of the distribution model, but it
should be remembered that the algorithm is just one part of the broader modeling
process; other factors, including selection of environmental variables (Section 3)
and application of a decision threshold (Section 5), are key elements of the
modeling process that affect model results and may be varied regardless of the
model algorithm being used. Nevertheless, studies comparing different modeling
algorithms have demonstrated substantial differences between predictions from
26
alternative methods. The importance of selecting an appropriate algorithm is
discussed below.
The most comprehensive model comparison to date was provided by Elith et al.
(2006). The authors compared 16 modeling methods using 226 species across
six regions of the world. All of the models included in the study were
implemented using presence-only data for calibration (some methods required
the use of pseudo-absence data), but model performance was assessed using
data on both presence and absence. These analyses found differences between
predictions from alternative methods, but also found that some methods
consistently outperformed others. In general, models classified as ‘best’ were
those that were able to identify complex relationships that existed in the data,
including interactions among environmental variables.
27
of models to simulate actual distributions by using statistical tests that reward
models for correctly classifying both presences and absences (see Section 5). In
contrast, Pearson et al. (2007) assessed predictive performance based only on
the model’s ability to predict observed presences, arguing that the purpose of the
modeling was to identify potential distributions (in which case use of absence
data in assessing performance is invalid since a site classified as absent still may
be environmentally suitable). The relative merits of aiming to predict actual
versus potential distributions were discussed in Section 2. We will also return to
the question of how to identify ‘best’ models when describing various statistical
approaches for assessing predictive performance in Section 5. However, the
important point is that it is not straightforward to identify which methods are best,
and it is therefore not possible to recommend use of one method over another.
28
of the model to predict the calibration data (i.e. calibration and test datasets are
identical). However, this approach makes it difficult to identify models that have
over-fit the calibration data (meaning the model is able to accurately classify the
calibration data, but the model performs poorly when predicting test data),
making it impossible for users to judge how well the model may perform when
making predictions (Araújo et al., 2005a). It is therefore preferable to use test
data that are different from the calibration data.
Ideally, test data would be collected independently from the data used to
calibrate the model. For example, Fleishman et al. (2002) modeled the
occurrence of butterfly species in Nevada, USA, using species inventory data
collected during the period 1996-1999, and then tested the models using data
collected from new sites during 2000-2001 (see Case Study 1 for a comparable
study). Other researchers have undertaken validation using independent data
from different regions (e.g. Beerling et al., 1995; Peterson, 2003), data at
different spatial resolution (e.g., Araújo et al., 2005b; Pearson et al., 2004), data
from different time periods (e.g., Araújo et al., 2005a), and data from surveys
conducted by other researchers (Elith et al., 2006).
However, in practice it may not be possible to obtain independent test data and it
is therefore common to partition the available data into calibration and test
datasets. Several strategies are available for partitioning data, the simplest being
a one-time split in which the available data are assigned to calibration and test
datasets either randomly (e.g., Pearson et al., 2002) or by dividing the data
spatially (e.g., Peterson and Shaw, 2003). The relative proportions of data
included in each data set are somewhat arbitrary, and dependent on the total
number of locality points available (though using 70% for calibration and 30% for
testing is common, following guidelines provided by Huberty (1994)). An
alternative to a one-time split is ‘bootstrapping’, whereby the data are split
multiple times. Bootstrapping methods sample the original set of data randomly
with replacement (i.e. the same occurrence record could be included in the test
data more than once). Multiple models are thus built, and in each case predictive
performance is assessed against the corresponding test data. Validation
statistics can then be reported as the mean and range from the set of bootstrap
samples (e.g., Buckland and Elston, 1993; Verbyla and Litaitis, 1989). An
approach similar to bootstrapping, but sampling without replacement (i.e. the
same occurrence record cannot be included in the test data more than once),
can also be applied and may be termed ‘randomization’ (Fielding and Bell, 1997).
Another useful data partitioning method is k-fold partitioning. Here, data are split
into k parts of roughly equal size (k > 2) and each part is used as a test set with
the other k-1 sets used for model calibration. Thus, if we select k = 5 then five
models will be calibrated and each model tested against the excluded test data.
Validation statistics are then reported as the mean and range from the set of k
tests (Fielding and Bell, 1997). An extreme form of k-fold partitioning, with k
equal to the number of occurrence localities, is recommended for use with very
29
low sample sizes (e.g., < 20; Pearson et al., 2007). This method is termed
‘jackknifing’ or ‘leave-one-out’ since each occurrence locality is excluded from
model calibration during one partition.
The confusion matrix is rather more straightforward than its name suggests, and
is alternatively termed an ‘error matrix’ or a ‘contingency table’. The confusion
matrix records the frequencies of each of the four possible types of prediction
from analysis of test data: (a) true positive (the model predicts that the species is
present and test data confirms this to be true), (b) false positive (the model
predicts presence but test data show absence), (c) false negative (the model
predicts absence but test data show presence), (d) true negative (the model
predicts and the test data show absence). Frequencies are commonly recorded
in a confusion matrix with the following form:
30
recorded present recorded absent
predicted
9 2
present
predicted
3 13
absent
The frequencies in the confusion matrix form the basis for a variety of different
statistical tests that can be used to assess model performance. Most of the
commonly used tests are described below. Terminology related to model
performance often varies from study to study and is sometimes not intuitive. In
particular, false negative predictions are commonly termed errors of ‘omission’,
whilst false positive predictions are termed errors of ‘commission’.
Figure 4. Diagram illustrating the four types of outcomes that are possible when assessing the
predictive performance of a species distribution model: true positive, false positive, false negative
and true negative. The diagram uses the same hypothetical actual and modeled distributions as
in Figure 3. Each instance of a symbol (x, □, ○, -) on the map depicts a site that has been
surveyed and presence or absence of the species recorded (it is assumed here that if a site falls
within the actual distribution then the species will be detected). These survey records constitute
the test data. Frequencies of each type of outcome are commonly entered into a confusion matrix
(see main text).
31
Test statistics derived from the confusion matrix
A simple measure of predictive performance that can be derived from the
confusion matrix is the proportion (or percentage) of test localities that are
correctly predicted, calculated as
(a + d ) /( a + b + c + d )
Accuracy and Kappa statistics use all values in the confusion matrix and
therefore require both presence and absence data. However, absence data are
often unavailable (e.g. when using specimens from museum collections) and are
inappropriate for use when the aim is to estimate the potential distribution (since
the environment may be suitable even though the species is absent).
When only presence records are used, the proportion of observed occurrences
correctly predicted can be calculated as
a /( a + c)
c /( a + c)
which is often termed ‘omission rate’ or ‘false positive fraction’. Note that these
two measures – sensitivity and omission rate – sum to 1. Thus, high sensitivity
means low omission, and low sensitivity means high omission. Although
sensitivity and omission rate avoid the use of absence records, a serious
disadvantage of these tests is that it is possible to achieve very high sensitivity
(and low omission) simply by predicting that the species is present at an
32
excessively large proportion of the study area. In short, it is possible to cheat: if
the model predicts the entire study area to be suitable, then sensitivity will equal
1, and omission rate will be zero. To avoid this problem, it is necessary to test the
statistical significance of a sensitivity or omission rate score.
To test for statistical significance, we ask whether the accuracy of our predictions
is greater than would be expected by chance. Imagine, for example, that we are
blindfolded and asked to throw darts at a map of our study area. The sites
identified by our random throws are then used as species’ occurrence localities
for model testing. The probability of landing darts in the area predicted by the
model to be suitable for the species is equal to the proportion of the study area
that is predicted as suitable. Thus, if the model predicts that the species will be
present in 40% of the study area, then our probability of successfully landing a
dart in the area predicted as suitable is 0.4.
We can apply the same logic to assess the statistical significance of a sensitivity
(or omission rate) score. In this case, we use an exact one-tailed binomial test (or
for larger sample sizes a chi-square test; for description of binomial and chi-
square tests see Zar, 1996) to calculate the probability of obtaining a sensitivity
result by chance alone (Anderson et al., 2002a). For example, suppose that the
model in Figure 4 predicts that 30% of the study area is suitable for the species.
The probability of success by chance alone for each test locality is therefore 0.3.
We can calculate from the confusion matrix that the sensitivity = 9/(9+3) = 0.75,
and we can use an exact one-tailed binomial test to calculate that the probability
of making nine or more successful predictions of presence by chance alone is
0.0017. We may therefore conclude that our result is statistically significant (p <
0.01).
33
Another statistic that can be derived from the confusion matrix is the proportion of
observed absences that are correctly predicted, calculated as
d /(b + d )
34
Table 4. Some published methods for setting thresholds of occurrence.
35
Many methods for setting thresholds can be implemented by calculating statistics
derived from the confusion matrix across the range of possible thresholds. For
example, sensitivity and specificity may be calculated at thresholds increasing in
increments of 0.01 from 0 to 1 (i.e. 0, 0.01, 0.02, 0.03…0.99, 1). As the threshold
increases, the proportion of the study area predicted to be suitable for the
species, or in which the species is predicted to be ‘present,’ will decrease.
Consequently, the proportion of observed presences that are correctly predicted
decreases (i.e. decreasing sensitivity) and the proportion of observed absences
that are correctly predicted increases (i.e. increasing specificity) (Figure 5A).
From these data we can select the threshold at which sensitivity and specificity
are equal (labeled a in Figure 5A) or at which their sum is maximized. Similarly, it
is common to calculate Kappa across the range of possible thresholds and to
select the threshold at which the statistic is maximized (Figure 5B).
Figure 5. Plots showing changes in test statistics as the threshold of occurrence is adjusted. A.
Decrease in sensitivity and increase in specificity as the threshold is increased. The threshold
labeled a corresponds to the specificity-sensitivity equality threshold. B. Changes in the Kappa
statistic as the threshold is adjusted. The threshold labeled b corresponds to that threshold at
which Kappa is maximized.
36
the best methods for setting thresholds included maximizing the sum of
sensitivity and specificity, using the average probability/suitability score, and
setting equal prevalence between the calibration data and the prediction (Table
4). Maximizing Kappa did not perform well, and use of an arbitrary fixed value
performed worst.
Methods that use only presence records for setting a threshold are required for
cases in which absence data are unavailable. Presence-only methods can also
be justified on the grounds that they avoid false absences (Section 3): it may be
argued that we should be primarily concerned with maximizing the number of
observed presences that are correctly predicted, rather than minimizing the
number of absences that are incorrectly predicted as presences (since some
absences may be recorded in apparently suitable environments; Pearson et al.,
2006). For example, Pearson et al. (2007) used a dataset comprising very few
presence-only records for geckos in Madagascar. Because confidence was high
that the localities and species identification were correct, and because these
species are not highly mobile and are therefore unlikely to be found in unsuitable
habitat (i.e. sink habitat; see section 2), omission of any occurrence record was
considered a clear model error. Therefore, the minimum predicted value
corresponding to an observed presence was selected as a threshold to ensure
zero omission. Distribution models thus predicted that many regions of the study
area were suitable although no presences had been detected there. This
approach suited the aim of the study, which was to prioritize regions for future
surveys by estimating the potential distribution (see Case Study 1).
Threshold-independent assessment
When model output is continuous, assessment of predictive performance using
statistics derived from the confusion matrix will be sensitive to the method used
to select a threshold for creating a binary prediction. Furthermore, if predictions
are binary, the assessment of performance does not take into account all of the
information provided by the model (Fielding and Bell, 1997). Therefore, it is often
useful to derive a test statistic that provides a single measure of predictive
performance across the full range of possible thresholds. This can be achieved
using a statistic known as AUC: the Area Under the Receiver Operating
Characteristic Curve.
37
The AUC test is derived from the Receiver Operating Characteristic (ROC)
Curve. The ROC curve is defined by plotting sensitivity against ‘1 – specificity’
across the range of possible thresholds (Figure 6A). Sensitivity and specificity
are used because these two measures take into account all four elements of the
confusion matrix (true and false presences and absences). It is conventional to
subtract specificity from 1 (i.e. 1 – specificity) so that both sensitivity and
specificity vary in the same direction when the decision threshold is adjusted
(Pearce and Ferrier, 2000). The ROC curve thus describes the relationship
between the proportion of observed presences correctly predicted (sensitivity)
and the proportion of observed absences incorrectly predicted (1 – specificity).
Therefore, a model that predicts perfectly will generate an ROC curve that
follows the left axis and top of the plot, whilst a model with predictions that are no
better than random (i.e. is unable to classify accurately sites at which the species
is present and absent) will generate a ROC curve that follows the 1:1 line (Figure
6A).
Figure 6. Example Receiver Operating Characteristic (ROC) Curves and illustrative frequency
distributions. A. ROC curves formed by plotting sensitivity against ‘1 – specificity’. Two ROC
curves are shown, the upper curve (red) signifying superior predictive ability. The dashed 1:1 line
signifies random predictive ability, whereby there is no ability to distinguish occupied and
unoccupied sites. B and C show example frequency distributions of probabilities predicted by a
model for observed ‘presences’ and ‘absences’. The results shown in B reveal good ability to
distinguish presence from absence, whilst results in C show more overlap between the frequency
distributions thus revealing poorer classification ability. The case shown in B would produce an
ROC curve similar to the upper (red) curve in A. The case shown in C would give an ROC curve
more like the lower (blue) curve in A.
38
AUC thus ranges from 0.5 for models that are no better than random to 1.0 for
models with perfect predictive ability. We can think of AUC in terms of the
frequency distributions of probabilities predicted for locations at which we have
empirical data on presence and absence (Figure 6, B and C). A high AUC score
reflects that the model can discriminate accurately between locations at which
the species is present or absent. In fact, AUC can be interpreted as the
probability that a model will correctly distinguish between a presence record and
an absence record if each record is selected randomly from the set of presences
and absences. Thus, an AUC value of 0.8 means the probability is 0.8 that a
record selected at random from the set of presences will have a predicted value
greater than a record selected at random from the set of absences (Fielding and
Bell, 1997; Pearce and Ferrier, 2000).
AUC is a test that uses both presence and absence records. However, Phillips et
al. (2006) have demonstrated how the test can be applied using randomly
selected ‘pseudo-absence’ records in lieu of observed absences. In this case,
AUC tests whether the model classifies presence more accurately than a random
prediction, rather than whether the model is able to accurately distinguish
presence from absence.
A number of different methods can be used to compute the AUC (Pearce and
Ferrier, 2000). Some distribution modeling programs automatically calculate the
AUC (e.g. Maxent; Table 3). The statistic can also be calculated using numerous
other free software packages (e.g. R, for free download see http://www.r-
project.org/).
If the aim of the modeling is to estimate the potential distribution (Section 2) then
presence-only assessment of model performance using sensitivity and statistical
significance is likely to be preferable. In this case we cannot test if the model is
correct (since we do not know the true potential distribution), but rather we test if
the model is useful. Our criteria for usefulness are that the model successfully
predicts presence in a high proportion of test localities (i.e., known occurrences)
whilst not predicting that an excessively large proportion of the study area is
suitable. Thus, a model that successfully predicts whether the species is present
at all test localities whilst classifying most of the study area as suitable may be
39
correct (the environment may truly be suitable throughout most of the study
area); however, the model is not useful because it is not more informative than a
random prediction.
40
Two alternative thresholds of occurrence were used: threshold = 1 (termed by the
authors “any model predicts”), and threshold = 10 (termed “all models predict”).
Raxworthy et al. (2003) thus demonstrated the potential for species’ distribution
models to be used to guide new field surveys toward areas in which the
probability of species presence was high. This approach takes advantage of the
type of model prediction illustrated by area 2 in Figure 3: the model identifies an
area that is environmentally similar to where the species has already been found,
but for which no occurrence data are available. The models can thus help to
address the Wallacean shortfall, by improving our knowledge of the distributions
of known species.
Raxworthy et al. (2003) also demonstrated that the models can help to address
the Linnean shortfall by guiding field surveys toward areas where species new to
science are most likely to be discovered. In this case the approach makes use of
the type of model prediction illustrated by area 3 in Figure 3: areas are identified
that are unoccupied by the species being modeled, but where closely-related
species that occupy similar environmental space are most likely to be found. By
surveying sites identified by the distribution models for known species,
Raxworthy et al. (2003) discovered seven new species, considerably greater
than the number that would usually be expected on the basis of similar survey
effort across a less-targeted area.
41
susceptibility to invasion. The approach makes use of the type of model
prediction illustrated by area 3 in Figure 3: areas are identified that are part of the
potential, but not actual, distribution. Thuiller et al. (2005) used this method to
identify parts of the world that are potentially susceptible to invasion by plant
species native to South Africa.
Thuiller and colleagues developed distribution models for 96 South African plant
taxa that are invasive in other regions of the globe. Species distribution data
were extracted from large databases of occurrence records that have been
collated for South Africa. Since the surveys incorporated within these databases
were fairly comprehensive, the authors argued that absences within the
databases are reliable and the modeling was thus undertaken using presence
and absence data. Four climate-related variables that are known to affect plant
physiology and growth were developed and used as input to the models. These
included two measures of temperature (growing degree days and temperature of
the coldest month) along with indexes of humidity and plant productivity. All the
analyses were undertaken at a resolution of 25x25 km, which was considered
sufficiently fine to identify environmental differences between regions at a global
scale. Generalized Additive Models (implemented using the Splus-based
BIOMOD application; Table 3) were used to build the distribution models.
The first step in the study was to model each species’ distribution based on its
native range in South Africa. Models were calibrated using 70% of the available
records for each species, with the remaining 30% retained for model testing. The
AUC validation test was applied using presence and absence test data. Because
AUC assesses predictive performance based on continuous model output, it was
not necessary to set a threshold of occurrence. Validation statistics for the test
data were generally very good, with a median AUC score across all 96 species of
0.94 (minimum = 0.68, maximum = 1.0).
The second step in the study was to project the calibrated models worldwide.
The accuracy of the global predictions was assessed for three example species
using presence-only records from their non-native distributions (for example, in
Europe, Australia and New Zealand). Absence records were not available for
these tests, so model performance was assessed using chi-square tests (see
section 5). For each of the species, predictions of potentially suitable areas
outside South Africa showed considerable agreement with observed records of
invasions (chi-square test, P<0.05).
In a further step, Thuiller and colleagues summed the probability surfaces for all
96 taxa to produce a global map for risk of invasion by species of South African
origin. Parts of the world most susceptible to invasion included six biodiversity
‘hotspots’, including the Mediterranean Basin, California Floristic Province, and
southwest Australia. This study demonstrates that species distribution modeling
can be a valuable tool for identifying sites prone to invasion. Such sites may be
42
prioritized for monitoring and quarantine measures can be put in place to help
avoid the establishment of invasive species.
Berry et al. (2002) modeled 54 species that were chosen to represent a range of
habitats common in Britain and Ireland. Species distribution data were obtained
for the whole of Europe (i.e. European extent) from range maps for European
plants, amphibians, butterflies and mammals. Since survey effort across Europe
is generally very high, areas where a species had not been recorded were
considered reliable measures of absence, and both presence and absence data
were therefore used in the modeling. Five environmental variables describing
temperature, precipitation and soil type were used. These variables were
generated using both current climate data and predictions of future climate from
a General Circulation Model (GCM). GCMs are complex simulations that predict
future climates using scenarios of greenhouse gas emissions. The environmental
variables were calculated at a coarse resolution (~50x50km) for Europe, and also
at a finer resolution (10x10km) for Britain and Ireland. The modeling algorithm
was an Artificial Neural Network (Table 3), which gave predictions of relative
suitability ranging from 0 to 1. These continuous predictions were converted into
binary predictions of presence and absence by applying a threshold of
occurrence that maximized the Kappa statistic.
An important part of Berry et al’s (2002) method was that calibration of the
distribution model was carried out at the European scale (large extent and coarse
resolution) and then the model was used to predict distributions in Britain and
Ireland (smaller extent and finer resolution). This approach ensured that when
distributions were predicted under future climate scenarios in Britain and Ireland,
the model was not required to extrapolate beyond the range of data for which it
was calibrated (since future climates in Britain and Ireland are expected to be
similar to conditions currently experienced elsewhere in Europe).
43
statistic was applied. Results from these tests revealed generally good model
performance, with 27 out of 54 species achieving Kappa scores >0.75, and only
7 of 54 species with Kappa scores <0.6.
The models calibrated for Europe were then used to predict distributions in
Britain and Ireland under current and projected future climates. Berry et al.
(2002) emphasized that they did not predict actual distributions, but rather
‘bioclimate envelopes’, or suitable climate space. It is important to remember that
actual future distributions will be determined by many factors that are not taken
into account in the modeling, including the ability of species to colonize areas
that become suitable. Nevertheless, the distribution models enabled each
species to be placed in one of three categories: those expected to lose suitable
climate space, those expected to gain suitable climate space, and those showing
little change. Species’ distribution modeling thus enables preliminary
assessments of the possible impacts of climate change to be made, providing
information that may be valuable in developing conservation policies to address
the threat.
ACKNOWLEDGEMENTS
Thorough comments from five anonymous reviewers greatly improved the
module. The module also benefitted significantly from editorial input by Ian
Harrison and the rest of the NCEP team. Extensive discussions with Robert
Anderson, Catherine Graham, Steven Phillips, Town Peterson, Chris Raxworthy,
Jorge Sóberon and members of the New York Species Distribution Modeling
Discussion Group greatly contributed to the module. I am also indebted to
comments and discussion by participants in courses I have taught through the
American Museum of Natural History, and the Global Biodiversity Information
Facility.
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